Nrf2 activation involves an oxidative-stress independent pathway in tetrafluoroethylcysteine-induced cytotoxicity

Toxicological Sciences

Volumn 86, Issue 2, 2005, Pages 354-364

  Ho, Han K ^a   White, Collin C ^a   Fernandez, Carolina ^a   Fausto, Nelson ^a   Kavanagh, Terrance J ^a   Nelson, Sidney D ^a   Bruschi, Sam A ^a  

^a UNIVERSITY OF WASHINGTON   (United States)

Author keywords

ER stress; Mitochondrial dysfunction; Nrf2; Oxidative stress; Tetrafluoroethylcysteine

Indexed keywords

ACONITATE HYDRATASE; ASPARTATE AMINOTRANSFERASE; CARDIOLIPIN; CYSTEINE DERIVATIVE; GLUTAMATE CYSTEINE LIGASE; GLUTATHIONE; GLUTATHIONE TRANSFERASE; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 153; GROWTH ARREST AND DNA DAMAGE INDUCIBLE PROTEIN 45; HEAT SHOCK PROTEIN 60; HEME OXYGENASE 1; MITOCHONDRIAL PROTEIN; OXOGLUTARATE DEHYDROGENASE; PROTEIN KINASE; REACTIVE OXYGEN METABOLITE; TETRAFLUOROETHYLENE; THIOL; TRANSCRIPTION FACTOR NRF2;

ANIMAL CELL; ARTICLE; CELL LINE; CELL NUCLEUS; CONTROLLED STUDY; CYTOSOL; CYTOTOXICITY; DATA ANALYSIS; ENDOPLASMIC RETICULUM; ENZYME SUBUNIT; GENE ACTIVATION; IN VITRO STUDY; LIVER TOXICITY; NEPHROTOXICITY; NONHUMAN; NUCLEOTIDE SEQUENCE; OXIDATIVE STRESS; PHOSPHORYLATION; PROTEIN MODIFICATION; TRANSCRIPTION REGULATION; TRANSLATION REGULATION;

ADENOSINE TRIPHOSPHATE; ANIMALS; CALCIUM; CELL LINE; CELL SURVIVAL; CYSTEINE; DNA-BINDING PROTEINS; GENE EXPRESSION PROFILING; GENE EXPRESSION REGULATION; GLUTATHIONE; HYDROCARBONS, FLUORINATED; HYDROGEN PEROXIDE; MICE; NF-E2-RELATED FACTOR 2; OLIGONUCLEOTIDE ARRAY SEQUENCE ANALYSIS; REVERSE TRANSCRIPTASE POLYMERASE CHAIN REACTION; RNA, MESSENGER; TRANS-ACTIVATORS;

ANIMALIA; MURINAE;

EID: 26444588758     PISSN: 10966080     EISSN: 10960929     Source Type: Journal    
DOI: 10.1093/toxsci/kfi205     Document Type: Article

References (37)

1. Botta, D., Franklin, C. C., White, C. C., Krejsa, C. M., Dabrowski, M. J., Pierce, R. H., Fausto, N., and Kavanagh, T. J. (2004). Glutamate-cysteine ligase attenuates TNF-induced mitochondrial injury and apoptosis. [i#Free Radic. Biol. Med.#1i] [b#37#1b], 632-642.
2. Bruschi, S. A., Lindsay, J. G., and Crabb, J. W. (1998). Mitochondrial stress protein recognition of inactivated dehydrogenases during mammalian cell death. [i#Proc. Natl. Acad. Sci. U.S.A.#1i] [b#95#1b], 13413-13418.
3. Bruschi, S. A., West, K. A., Crabb, J. W., Gupta, R. S., and Stevens, J. L. (1993). Mitochondrial HSP60 (P1 protein) and a HSP70-like protein (mortalin) are major targets for modification during S-(1,1,2,2-tetrafluoroethyl)-L-cysteine-induced nephrotoxicity. [i#J. Biol. Chem.#1i] [b#268#1b], 23157-23161.
4. Buckley, B. J., Marshall, Z. M., and Whorton, A. R. (2003). Nitric oxide stimulates Nrf2 nuclear translocation in vascular endothelium. [i#Biochem. Biophys. Res. Commun.#1i] [b#307#1b], 939-973.
5. Chen, C., Pung, D., Leong, V., Hebbar, V., Shen, G., Nair, S., Li, W., and Tony Kong, A. N. (2004). Induction of detoxifying enzymes by garlic organosulfur compounds through transcription factor Nrf2: Effect of chemical structure and stress signals. [i#Free Radic. Biol. Med.#1i] [b#37#1b], 1578-1590.
6. Cooper, A. J., Bruschi, S. A., and Anders, M. W. (2002). Toxic, halogenated cysteine S-conjugates and targeting of mitochondrial enzymes of energy metabolism. [i#Biochem. Pharmacol.#1i] [b#64#1b], 553-564.
7. Cullinan, S. B., and Diehl, J. A. (2004). PERK-dependent activation of Nrf2 contributes to redox homeostasis and cell survival following endoplasmic reticulum stress. [i#J. Biol. Chem.#1i] [b#279#1b], 20108-20117.
8. Cullinan, S. B., Zhang, D., Hannink, M., Arvisais, E., Kaufman, R. J., and Diehl, J. A. (2003). Nrf2 is a direct PERK substrate and effector of PERK-dependent cell survival. [i#Mol. Cell. Biol.#1i] [b#23#1b], 7198-7209.
9. Dietze, E. C., Schafer, A., Omichinski, J. G., and Nelson, S. D. (1997). Inactivation of glyceraldehyde-3-phosphate dehydrogenase by a reactive metabolite of acetaminophen and mass spectral characterization of an arylated active site peptide. [i#Chem. Res. Toxicol.#1i] [b#10#1b], 1097-1103.
10. Groves, C. E., Lock, E. A., and Schnellmann, R. G. (1991). Role of lipid peroxidation in renal proximal tubule cell death induced by haloalkene cysteine conjugates. [i#Toxicol. Appl. Pharmacol.#1i] [b#107#1b], 54-62.
11. Harriman, J. F., Liu, X. L., Aleo, M. D., Machaca, K., and Schnellmann, R. G. (2002). Endoplasmic reticulum Ca(2+) signaling and calpains mediate renal cell death. [i#Cell Death Differ.#1i] [b#9#1b], 734-741.
12. Ho, H. K., Hu, Z. H., Tzung, S. P., Hockenbery, D. M., Fausto, N., Nelson, S. D., and Bruschi, S. A. (2005). BCL-xL overexpression effectively protects against tetrafluoroethylcysteine-induced intramitochondrial damage and cell death. [i#Biochem. Pharmacol.#1i] [b#69#1b], 147-157.
13. Itoh, K., Tong, K. I., and Yamamoto, M. (2004). Molecular mechanism activating Nrf2-Keap1 pathway in regulation of adaptive response to electrophiles. [i#Free Radic. Biol. Med.#1i] [b#36#1b], 1208-1213.
14. Itoh, K., Wakabayashi, N., Katoh, Y., Ishii, T., O'Connor, T., and Yamamoto, M. (2003). Keap1 regulates both cytoplasmic-nuclear shuttling and degradation of Nrf2 in response to electrophiles. [i#Genes Cells#1i] [b#8#1b], 379-391.
15. Jaiswal, A. K. (2004). Nrf2 signaling in coordinated activation of antioxidant gene expression. [i#Free Radic. Biol. Med.#1i] [b#36#1b], 1199-1207.
16. James, E. A., Gygi, S. P., Adams, M. L., Pierce, R. H., Fausto, N., Aebersold, R. H., Nelson, S. D., and Bruschi, S. A. (2002). Mitochondrial aconitase modification, functional inhibition, and evidence for a supramolecular complex of the TCA cycle by the renal toxicant S-(1,1,2,2-tetrafluoroethyl)-L-cysteine. [i#Biochemistry#1i] [b#41#1b], 6789-6797.
17. Kang, M. I., Kobayashi, A., Wakabayashi, N., Kim, S. G., and Yamamoto, M. (2004). Scaffolding of Keap1 to the actin cytoskeleton controls the function of Nrf2 as key regulator of cytoprotective phase 2 genes. [i#Proc. Natl. Acad. Sci. U.S.A.#1i] [b#101#1b], 2046-2051.
18. Katsuoka, F., Motohashi, H., Engel, J. D., and Yamamoto, M. (2005). Nrf2 transcriptionally activates the mafG gene through an antioxidant response element. [i#J. Biol. Chem.#1i] [b#280#1b], 4483-4490.
19. Lee, J. M., and Johnson, J. A. (2004). An important role of Nrf2-ARE pathway in the cellular defense mechanism. [i#J. Biochem. Mol. Biol.#1i] [b#37#1b], 139-143.
20. Lee, J. M., Shih, A. Y., Murphy, T. H., and Johnson, J. A. (2003). NF-E2-related factor-2 mediates neuroprotection against mitochondrial complex I inhibitors and increased concentrations of intracellular calcium in primary cortical neurons. [i#J. Biol. Chem.#1i] [b#278#1b], 37948-37956.
21. Leist, M., Single, B., Castoldi, A. F., Kuhnle, S., and Nicotera, P. (1997). Intracellular adenosine triphosphate (ATP) concentration: A switch in the decision between apoptosis and necrosis. [i#J. Exp. Med.#1i] [b#185#1b], 1481-1486.
22. Leist, M., Single, B., Naumann, H., Fava, E., Simon, B., Kuhnle, S., and Nicotera, P. (1999). Inhibition of mitochondrial ATP generation by nitric oxide switches apoptosis to necrosis. [i#Exp. Cell Res.#1i] [b#249#1b] 396-403.
23. Levonen, A. L., Landar, A., Ramachandran, A., Ceaser, E. K., Dickinson, D. A., Zanoni, G., Morrow, J. D., and Darley-Usmar, V. M. (2004). Cellular mechanisms of redox cell signalling: Role of cysteine modification in controlling antioxidant defences in response to electrophilic lipid oxidation products. [i#Biochem. J.#1i] [b#378#1b], 373-382.
24. Lieberthal, W., Menza, S. A., and Levine, J. S. (1998). Graded ATP depletion can cause necrosis or apoptosis of cultured mouse proximal tubular cells. [i#Am. J. Physiol.#1i] [b#274#1b], F315-F327.
25. Liu, X. M., Peyton, K. J., Ensenat, D., Wang, H., Schafer, A. I., Alam, J., and Durante, W. (2005). Endoplasmic reticulum stress stimulates heme oxygenase-1 gene expression in vascular smooth muscle. Role in cell survival. [i#J. Biol. Chem.#1i] [b#280#1b], 872-877.
26. Lock, E. A., and Ishmael, J. (1998). The nephrotoxicity and hepatotoxicity of 1,1,2,2-tetrafluoroethyl-L-cysteine in the rat. [i#Arch. Toxicol.#1i] [b#72#1b], 347-354.
27. Nakaso, K., Yano, H., Fukuhara, Y., Takeshima, T., Wada-Isoe, K., and Nakashima, K. (2003). PI3K is a key molecule in the Nrf2-mediated regulation of antioxidative proteins by hemin in human neuroblastoma cells. [i#FEBS Lett.#1i] [b#546#1b], 181-184.
28. Nguyen, T., Sherratt, P. J., and Pickett, C. B. (2003). Regulatory mechanisms controlling gene expression mediated by the antioxidant response element. [i#Annu. Rev. Pharmacol. Toxicol.#1i] [b#43#1b], 233-260.
29. Numazawa, S., Ishikawa, M., Yoshida, A., Tanaka, S., and Yoshida, T. (2003). Atypical protein kinase C mediates activation of NF-E2-related factor 2 in response to oxidative stress. [i#Am. J. Physiol. Cell Physiol.#1i] [b#285#1b], C334-C342.
30. Numazawa, S., and Yoshida, T. (2004). Nrf2-dependent gene expressions: A molecular toxicological aspect. [i#J. Toxicol. Sci.#1i] [b#29#1b], 81-89.
31. Pierce, R. H., Franklin, C. C., Campbell, J. S., Tonge, R. P., Chen, W., Fausto, N., Nelson, S. D., and Bruschi, S. A. (2002). Cell culture model for acetaminophen-induced hepatocyte death [i#in vivo. Biochem. Pharmacol.#1i] [b#64#1b], 413-424.
32. Sakurai, A., Nishimoto, M., Himeno, S., Imura, N., Tsujimoto, M., Kunimoto, M., and Hara, S. (2005). Transcriptional regulation of thioredoxin reductase 1 expression by cadmium in vascular endothelial cells: Role of NF-E2-related factor-2. [i#J. Cell Physiol.#1i] [b#203#1b], 529-537.
33. Schnellmann, R. G., and Williams, S. W. (1998). Proteases in renal cell death: Calpains mediate cell death produced by diverse toxicants. [i#Ren. Fail.#1i] [b#20#1b], 679-686.
34. Wolfgang, C. D., Chen, B. P., Martindale, J. L., Holbrook, N. J., and Hai, T. (1997). gadd153/Chop10, a potential target gene of the transcriptional repressor ATF3. [i#Mol. Cell. Biol.#1i] [b#17#1b], 6700-6707.
35. Wu, J. C., Merlino, G., Cveklova, K., Mosinger, B., Jr., and Fausto, N. (1994). Autonomous growth in serum-free medium and production of hepatocellular carcinomas by differentiated hepatocyte lines that overexpress transforming growth factor alpha 1. [i#Cancer Res.#1i] [b#54#1b] 5964-5973.
36. Yu, R., Chen, C., Mo, Y. Y., Hebbar, V., Owuor, E. D., Tan, T. H., and Kong, A. N. (2000). Activation of mitogen-activated protein kinase pathways induces antioxidant response element-mediated gene expression via a Nrf2-dependent mechanism. [i#J. Biol. Chem.#1i] [b#275#1b], 39907-39913.
37. Zhang, D. D., and Hannink M. (2003). Distinct cysteine residues in Keap1 are required for Keap1-dependent ubiquitination of Nrf2 and for stabilization of Nrf2 by chemopreventive agents and oxidative stress. [i#Mol. Cell. Biol.#1i] [b#23#1b], 8137-8151.